Seeing faces is necessary for face-domain formation

Abstract

Here we report that monkeys raised without exposure to faces did not develop face domains, but did develop domains for other categories and did show normal retinotopic organization, indicating that early face deprivation leads to a highly selective cortical processing deficit. Therefore, experience must be necessary for the formation (or maintenance) of face domains. Gaze tracking revealed that control monkeys looked preferentially at faces, even at ages prior to the emergence of face domains, but face-deprived monkeys did not, indicating that face looking is not innate. A retinotopic organization is present throughout the visual system at birth, so selective early viewing behavior could bias category-specific visual responses toward particular retinotopic representations, thereby leading to domain formation in stereotyped locations in inferotemporal cortex, without requiring category-specific templates or biases. Thus, we propose that environmental importance influences viewing behavior, viewing behavior drives neuronal activity, and neuronal activity sculpts domain formation.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Faces>objects and hands>objects activations in control and face-deprived monkeys.
Figure 2: Quantification of face and hand activations in control and face-deprived monkeys.
Figure 3: Activations to bodies minus scenes.
Figure 4: Eccentricity organization in control and face-deprived monkeys.
Figure 5: Looking behavior of control and face-deprived monkeys.

References

  1. 1

    McKone, E., Crookes, K., Jeffery, L. & Dilks, D.D. A critical review of the development of face recognition: experience is less important than previously believed. Cogn. Neuropsychol. 29, 174–212 (2012).

  2. 2

    McKone, E., Crookes, K. & Kanwisher, N. in The Cognitive Neurosciences 4th edn. (ed. Gazzaniga, M.) 467–482 (MIT Press, 2009).

  3. 3

    Goren, C.C., Sarty, M. & Wu, P.Y. Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics 56, 544–549 (1975).

  4. 4

    Johnson, M.H., Dziurawiec, S., Ellis, H. & Morton, J. Newborns' preferential tracking of face-like stimuli and its subsequent decline. Cognition 40, 1–19 (1991).

  5. 5

    Mendelson, M.J., Haith, M.M. & Goldman-Rakic, P.S. Face scanning and responsiveness to social cues in infant rhesus monkeys. Dev. Psychol. 18, 222–228 (1982).

  6. 6

    Cassia, V.M., Turati, C. & Simion, F. Can a nonspecific bias toward top-heavy patterns explain newborns' face preference? Psychol. Sci. 15, 379–383 (2004).

  7. 7

    Turati, C., Simion, F., Milani, I. & Umiltà, C. Newborns' preference for faces: what is crucial? Dev. Psychol. 38, 875–882 (2002).

  8. 8

    Tanaka, J.W. & Farah, M.J. Parts and wholes in face recognition. Q. J. Exp. Psychol. A 46, 225–245 (1993).

  9. 9

    Young, A.W., Hellawell, D. & Hay, D.C. Configurational information in face perception. Perception 16, 747–759 (1987).

  10. 10

    Stryker, M.P. et al. in Neurobiology of Neocortex (eds. Rakic, P. & Singer, W.) 115–136 (Wiley, 1988).

  11. 11

    Cohen, L. & Dehaene, S. Specialization within the ventral stream: the case for the visual word form area. Neuroimage 22, 466–476 (2004).

  12. 12

    Aguirre, G.K., Zarahn, E. & D'Esposito, M. An area within human ventral cortex sensitive to 'building' stimuli: evidence and implications. Neuron 21, 373–383 (1998).

  13. 13

    Srihasam, K., Vincent, J.L. & Livingstone, M.S. Novel domain formation reveals proto-architecture in inferotemporal cortex. Nat. Neurosci. 17, 1776–1783 (2014).

  14. 14

    Levy, I., Hasson, U., Avidan, G., Hendler, T. & Malach, R. Center–periphery organization of human object areas. Nat. Neurosci. 4, 533–539 (2001).

  15. 15

    Malach, R., Levy, I. & Hasson, U. The topography of high-order human object areas. Trends Cogn. Sci. 6, 176–184 (2002).

  16. 16

    Martin, A., Wiggs, C.L., Ungerleider, L.G. & Haxby, J.V. Neural correlates of category-specific knowledge. Nature 379, 649–652 (1996).

  17. 17

    Ishai, A., Ungerleider, L.G., Martin, A., Schouten, J.L. & Haxby, J.V. Distributed representation of objects in the human ventral visual pathway. Proc. Natl. Acad. Sci. USA 96, 9379–9384 (1999).

  18. 18

    Arcaro, M.J. & Livingstone, M.S. A hierarchical, retinotopic proto-organization of the primate visual system at birth. Elife 6, e26196 (2017).

  19. 19

    Harlow, H.F. & Suomi, S.J. Social recovery by isolation-reared monkeys. Proc. Natl. Acad. Sci. USA 68, 1534–1538 (1971).

  20. 20

    Livingstone, M.S. et al. Development of the macaque face-patch system. Nat. Commun. 8, 14897 (2017).

  21. 21

    Tsao, D.Y., Freiwald, W.A., Knutsen, T.A., Mandeville, J.B. & Tootell, R.B. Faces and objects in macaque cerebral cortex. Nat. Neurosci. 6, 989–995 (2003).

  22. 22

    Pinsk, M.A., DeSimone, K., Moore, T., Gross, C.G. & Kastner, S. Representations of faces and body parts in macaque temporal cortex: a functional-MRI study. Proc. Natl. Acad. Sci. USA 102, 6996–7001 (2005).

  23. 23

    Kornblith, S., Cheng, X., Ohayon, S. & Tsao, D.Y. A network for scene processing in the macaque temporal lobe. Neuron 79, 766–781 (2013).

  24. 24

    Arcaro, M.J. & Livingstone, M.S. Retinotopic organization of scene areas in macaque inferior temporal cortex. J. Neurosci. 37, 7373–7389 (2017).

  25. 25

    Nasr, S. et al. Scene-selective cortical regions in human and nonhuman primates. J. Neurosci. 31, 13771–13785 (2011).

  26. 26

    Arcaro, M.J., Pinsk, M.A., Li, X. & Kastner, S. Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study. J. Neurosci. 31, 2064–2078 (2011).

  27. 27

    Janssens, T., Zhu, Q., Popivanov, I.D. & Vanduffel, W. Probabilistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex. J. Neurosci. 34, 10156–10167 (2014).

  28. 28

    Kolster, H. et al. Visual field map clusters in macaque extrastriate visual cortex. J. Neurosci. 29, 7031–7039 (2009).

  29. 29

    Lafer-Sousa, R. & Conway, B.R. Parallel, multistage processing of colors, faces, and shapes in macaque inferior temporal cortex. Nat. Neurosci. 16, 1870–1878 (2013).

  30. 30

    Hasson, U., Levy, I., Behrmann, M., Hendler, T. & Malach, R. Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34, 479–490 (2002).

  31. 31

    Chan, A.W., Kravitz, D.J., Truong, S., Arizpe, J. & Baker, C.I. Cortical representations of bodies and faces are strongest in commonly experienced configurations. Nat. Neurosci. 13, 417–418 (2010).

  32. 32

    de Haas, B. et al. Perception and processing of faces in the human brain is tuned to typical feature locations. J. Neurosci. 36, 9289–9302 (2016).

  33. 33

    Issa, E.B. & DiCarlo, J.J. Precedence of the eye region in neural processing of faces. J. Neurosci. 32, 16666–16682 (2012).

  34. 34

    Golarai, G., Liberman, A., Yoon, J.M. & Grill-Spector, K. Differential development of the ventral visual cortex extends through adolescence. Front. Hum. Neurosci. 3, 80 (2010).

  35. 35

    Natu, V.S. et al. Development of neural sensitivity to face identity correlates with perceptual discriminability. J. Neurosci. 36, 10893–10907 (2016).

  36. 36

    Pascalis, O., de Haan, M. & Nelson, C.A. Is face-processing species-specific during the first year of life? Science 296, 1321–1323 (2002).

  37. 37

    Deen, B. et al. Organization of high-level visual cortex in human infants. Nat. Commun. 8, 13995 (2017).

  38. 38

    Ponce, C.R., Hartmann, T.S. & Livingstone, M.S. End-stopping predicts curvature tuning along the ventral stream. J. Neurosci. 37, 648–659 (2017).

  39. 39

    Ferrari, P.F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4, e302 (2006).

  40. 40

    Meltzoff, A.N. & Moore, M.K. Newborn infants imitate adult facial gestures. Child Dev. 54, 702–709 (1983).

  41. 41

    Turati, C., Macchi Cassia, V., Simion, F. & Leo, I. Newborns' face recognition: role of inner and outer facial features. Child Dev. 77, 297–311 (2006).

  42. 42

    Oostenbroek, J. et al. Comprehensive longitudinal study challenges the existence of neonatal imitation in humans. Curr. Biol. 26, 1334–1338 (2016).

  43. 43

    James, W. The Principles of Psychology (H. Holt and Company, 1890).

  44. 44

    Sugita, Y. Face perception in monkeys reared with no exposure to faces. Proc. Natl. Acad. Sci. USA 105, 394–398 (2008).

  45. 45

    Kanwisher, N. Functional specificity in the human brain: a window into the functional architecture of the mind. Proc. Natl. Acad. Sci. USA 107, 11163–11170 (2010).

  46. 46

    Bushnell, I.W.R. Mother's face recognition in newborn infants: learning and memory. Infant Child Dev. 10, 67–74 (2001).

  47. 47

    Hebb, D.O. The Organization of Behavior; a Neuropsychological Theory (Wiley, 1949).

  48. 48

    Livingstone, M.S. Ocular dominance columns in New World monkeys. J. Neurosci. 16, 2086–2096 (1996).

  49. 49

    Wiesel, T.N. & Hubel, D.H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).

  50. 50

    Blasdel, G., Obermayer, K. & Kiorpes, L. Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys. Vis. Neurosci. 12, 589–603 (1995).

  51. 51

    Willenbockel, V. et al. The SHINE toolbox for controlling low-level image properties. J. Vis. 10, 653 (2010).

  52. 52

    Leite, F.P. et al. Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. Neuroimage 16, 283–294 (2002).

  53. 53

    Vanduffel, W. et al. Visual-motion processing investigated using contrast agent-enhanced fMRI in awake, behaving monkeys. Neuron 32, 565–577 (2001).

  54. 54

    Wass, S.V., Smith, T.J. & Johnson, M.H. Parsing eye-tracking data of variable quality to provide accurate fixation-duration estimates in infants and adults. Behav. Res. Methods 45, 229–250 (2013).

  55. 55

    Kolster, H., Janssens, T., Orban, G.A. & Vanduffel, W. The retinotopic organization of macaque occipitotemporal cortex anterior to V4 and caudoventral to the middle temporal (MT) cluster. J. Neurosci. 34, 10168–10191 (2014).

  56. 56

    Gandhi, S.P., Heeger, D.J. & Boynton, G.M. Spatial attention affects brain activity in human primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 3314–3319 (1999).

  57. 57

    Martínez, A. et al. Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat. Neurosci. 2, 364–369 (1999).

  58. 58

    Somers, D.C., Dale, A.M., Seiffert, A.E. & Tootell, R.B. Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 1663–1668 (1999).

  59. 59

    Tsao, D.Y., Moeller, S. & Freiwald, W.A. Comparing face patch systems in macaques and humans. Proc. Natl. Acad. Sci. USA 105, 19514–19519 (2008).

  60. 60

    Logothetis, N.K., Guggenberger, H., Peled, S. & Pauls, J. Functional imaging of the monkey brain. Nat. Neurosci. 2, 555–562 (1999).

  61. 61

    Cox, R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

  62. 62

    Friston, K.J., Frith, C.D., Turner, R. & Frackowiak, R.S. Characterizing evoked hemodynamics with fMRI. Neuroimage 2, 157–165 (1995).

  63. 63

    Van Essen, D.C. et al. An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 8, 443–459 (2001).

Download references

Acknowledgements

We thank A. Schapiro and D. Tsao for comments on the manuscript. This work was supported by US National Institutes of Health (NIH) grants R01EY25670 (M.S.L.), R01EY16187 (M.S.L.), F32EY24187 (J.L.V.), and P30EY12196 (M.S.L.), and a William Randolph Hearst Fellowship (M.J.A.). This research was carried out in part at the Athinoula A. Martinos Center for Biomedical Imaging at the Massachusetts General Hospital, using resources provided by the Center for Functional Neuroimaging Technologies, a P41 Biotechnology Resource Grant (P41EB015896) supported by the National Institute of Biomedical Imaging and Bioengineering (NIBIB), NIH, and a NIH Shared Instrumentation Grant (S10RR021110).

Author information

All authors scanned and reared the monkeys; P.F.S. trained the monkeys; M.S.L., M.J.A., and P.F.S. analyzed the data; and M.S.L. wrote the paper.

Correspondence to Margaret S Livingstone.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Subsets of the images used for the scan sessions in Figures 1 & 2.

The stimuli were single large (~10 degrees across) images of monkey faces, familiar objects, monkey hands, or gloved human hands on a pink-noise background; each image subtended 20 x 20 degrees of visual angle.

Supplementary Figure 2 Analysis of gaze direction during stimulus blocks included in analysis.

(top left) Percent of block time that each monkey spent looking within 5° of the central fixation spot during stimulus-presentation blocks accepted for analysis for each category for each scan session, as indicated; different symbols indicate different monkeys, as in Figure 2c legend. (top right) Averages of all images from each category with 5° radius indicated in white. (bottom) Heat maps showing normalized and smoothed average total gaze time at each location on the screen averaged over accepted blocks for each category for example scan sessions from each monkey; maps are overlain on darkened examples of images from that category. Even for session B6 295, which had the lowest percent fixation, the gaze pattern was similar between categories and to that of other monkeys. Slight differences in centering of gaze are due to differences in calibration between sessions. Monitoring gaze direction in the scanner was less accurate than in the free-viewing situation because of longer eye-to-camera distance and less optimal camera angle.

Supplementary Figure 3 Average percent signal change in the same CIT and AIT ROIs as in Figure 2.

Percent signal change to faces (red), hands (green), or objects (blue) as a function of ventrolateral to dorsomedial distance along an anatomically defined CIT ROI (upper graphs) or an AIT ROI (lower graphs) extending from the crown of the lower lip of the STS to the upper bank of the STS (dotted outlines on the B5 face map in Figure 2). Shading indicates sem. Data were averaged over all sessions and both hemispheres of all three control monkeys that were scanned multiple times (left) and all three face-deprived monkeys (right). Activations were averaged across the AP dimension of the ROI to give an average response as a function of mediolateral location.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 and Supplementary Table 1 (PDF 898 kb)

Life Sciences Reporting Summary (PDF 221 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arcaro, M., Schade, P., Vincent, J. et al. Seeing faces is necessary for face-domain formation. Nat Neurosci 20, 1404–1412 (2017). https://doi.org/10.1038/nn.4635

Download citation

Further reading